Biophys J, October 1998, p. 1828-1835, Vol. 75, No. 4

Loss of Shaker K Channel Conductance in 0 K⁺ Solutions: Role of the Voltage Sensor

Department of Physiology, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104 USA

In potassium-free solutions some types of K channels enter a long-lasting nonconducting or "defunct" state. It is known that Shaker K channels must open in K⁺-free solutions to become defunct. Gating current studies presented here indicate an abnormal conformation in the defunct state that restricts S4 movement and alters its kinetics. Thus an abnormality initiated in the P region spreads to the gating apparatus. We find that channels most readily become defunct on repolarization to an intermediate voltage, thus prolonging occupancy of one of the several intermediate closed states. The state dependence of becoming defunct was further dissected by using the gating mutant L382A. Simply closing this channel at 0 mV (reversing the last activation step) does not make the mutant channel defunct. Instead, it is necessary to move further left (more fully closed) in the activation sequence. This was confirmed with ShIR experiments showing that channels become defunct only if there is inward gating charge movement. Rapid transit through the intermediate states, achieved at very negative voltage, is relatively ineffective at making channels defunct. Several mutations that removed C-type inactivation also made the channels resistant to becoming defunct. Our results show that normal gating current cannot be stably recorded in the absence of K⁺.

Biophys J, October 1998, p. 1828-1835, Vol. 75, No. 4
© 1998 by the Biophysical Society   0006-3495/98/10/1828/08  $2.00

This article has been cited by other articles:

				G. Klement, J. Nilsson, P. Arhem, and F. Elinder A Tyrosine Substitution in the Cavity Wall of a K Channel Induces an Inverted Inactivation Biophys. J., April 15, 2008; 94(8): 3014 - 3022. [Abstract] [Full Text] [PDF]

				F. Gomez-Lagunas Stability of the Shab K+ Channel Conductance in 0 K+ Solutions: The Role of the Membrane Potential Biophys. J., December 15, 2007; 93(12): 4197 - 4208. [Abstract] [Full Text] [PDF]

				I. Schroeder and U.-P. Hansen Saturation and Microsecond Gating of Current Indicate Depletion-induced Instability of the MaxiK Selectivity Filter J. Gen. Physiol., July 1, 2007; 130(1): 83 - 97. [Abstract] [Full Text] [PDF]

				Y. S. Goo, W. Lim, and K. S. Elmslie Ca2+ Enhances U-Type Inactivation of N-Type (CaV2.2) Calcium Current in Rat Sympathetic Neurons J Neurophysiol, September 1, 2006; 96(3): 1075 - 1083. [Abstract] [Full Text] [PDF]

				E. C. Ray and C. Deutsch A Trapped Intracellular Cation Modulates K+ Channel Recovery From Slow Inactivation J. Gen. Physiol., July 31, 2006; 128(2): 203 - 217. [Abstract] [Full Text] [PDF]

				H. Gang and S. Zhang Na+ Permeation and Block of hERG Potassium Channels J. Gen. Physiol., June 26, 2006; 128(1): 55 - 71. [Abstract] [Full Text] [PDF]

				R. A. Piskorowski and R. W. Aldrich Relationship between Pore Occupancy and Gating in BK Potassium Channels J. Gen. Physiol., April 24, 2006; 127(5): 557 - 576. [Abstract] [Full Text] [PDF]

				M. N. Krishnan, J.-P. Bingham, S. H. Lee, P. Trombley, and E. Moczydlowski Functional Role and Affinity of Inorganic Cations in Stabilizing the Tetrameric Structure of the KcsA K+ Channel J. Gen. Physiol., August 29, 2005; 126(3): 271 - 283. [Abstract] [Full Text] [PDF]

				O. Babich, D. Isaev, and R. Shirokov Role of extracellular Ca2+ in gating of CaV1.2 channels J. Physiol., June 15, 2005; 565(3): 709 - 715. [Abstract] [Full Text] [PDF]

				L. Song, A. Seeger, and J. Santos-Sacchi On Membrane Motor Activity and Chloride Flux in the Outer Hair Cell: Lessons Learned from the Environmental Toxin Tributyltin Biophys. J., March 1, 2005; 88(3): 2350 - 2362. [Abstract] [Full Text] [PDF]

				T. Haug, R. Olcese, L. Toro, and E. Stefani Regulation of K+ Flow by a Ring of Negative Charges in the Outer Pore of BKCa Channels. Part II: Neutralization of Aspartate 292 Reduces Long Channel Openings and Gating Current Slow Component J. Gen. Physiol., July 26, 2004; 124(2): 185 - 197. [Abstract] [Full Text] [PDF]

				C. Domene, A. Grottesi, and M. S. P. Sansom Filter Flexibility and Distortion in a Bacterial Inward Rectifier K+ Channel: Simulation Studies of KirBac1.1 Biophys. J., July 1, 2004; 87(1): 256 - 267. [Abstract] [Full Text] [PDF]

				J. T. Sack, R. W. Aldrich, and W. F. Gilly A Gastropod Toxin Selectively Slows Early Transitions in the Shaker K Channel's Activation Pathway J. Gen. Physiol., June 1, 2004; 123(6): 685 - 696. [Abstract] [Full Text] [PDF]

				F. Gomez-Lagunas, C. V.F. Batista, T. Olamendi-Portugal, M. E. Ramirez-Dominguez, and L. D. Possani Inhibition of the Collapse of the Shaker K+ Conductance by Specific Scorpion Toxins J. Gen. Physiol., February 23, 2004; 123(3): 265 - 279. [Abstract] [Full Text] [PDF]

				I. I. Pottosin and M. Martinez-Estevez Regulation of the Fast Vacuolar Channel by Cytosolic and Vacuolar Potassium Biophys. J., February 1, 2003; 84(2): 977 - 986. [Abstract] [Full Text] [PDF]

				C. M. Armstrong Distinguishing surface effects of calcium ion from pore-occupancy effects in Na+ channels PNAS, March 30, 1999; 96(7): 4158 - 4163. [Abstract] [Full Text] [PDF]